Urinary Polycyclic Aromatic Hydrocarbon Metabolites Are Associated with Biomarkers of Chronic Endocrine Stress, Oxidative Stress, and Inflammation in Adolescents: FLEHS-4 (2016–2020)
Abstract
:1. Introduction
2. Materials and Methods
2.1. Study Population
2.2. Data Collection
2.3. Analysis of Urinary PAH Metabolites and Urinary Specific Gravity
2.4. Analysis of 8-oxo-7,8-dihydro-2’-deoxyguanosine (8-oxodG) in Urine
2.5. Hair Sample Collection and Hair Cortisol Measurement
2.6. Total and Differential Leucocyte Count in Peripheral Blood
2.7. Statistical Analysis
3. Results
3.1. Study Population Characteristics
3.2. Associations between OH-PAHs and Effect Markers
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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Characteristics | All (n = 393) | % | Boys (n = 183) | % | Girls (n = 210) | % | p-Value |
---|---|---|---|---|---|---|---|
Age (years) | 0.855 | ||||||
<14.5 | 103 | 26.2 | 46 | 25.1 | 57 | 27.1 | |
14.5−15.5 | 258 | 65.6 | 121 | 66.1 | 137 | 65.2 | |
>15.5 | 32 | 8.1 | 16 | 8.7 | 16 | 7.6 | |
Perceived income adequacy | 0.668 | ||||||
Difficult | 111 | 28.2 | 53 | 29 | 58 | 27.6 | |
Rather easy | 125 | 31.8 | 61 | 33.3 | 64 | 30.5 | |
Easy–very easy | 151 | 38.4 | 66 | 36.1 | 85 | 40.5 | |
Missing | 6 | 1.5 | 3 | 1.6 | 3 | 1.4 | |
Area Deprivation Index | 0.180 | ||||||
0−5.3% | 94 | 23.9 | 40 | 21.9 | 54 | 25.7 | |
5.4−9.3% | 99 | 25.2 | 41 | 22.4 | 58 | 27.6 | |
9.4−15.5% | 101 | 25.7 | 47 | 25.6 | 54 | 25.7 | |
>15.5% | 99 | 25.2 | 55 | 30.1 | 44 | 21 | |
Body Mass Index a | 0.053 | ||||||
Underweight | 32 | 8.1 | 15 | 8.2 | 17 | 8.1 | |
Normal weight | 285 | 72.5 | 142 | 77.6 | 143 | 68.1 | |
Overweight, obese | 76 | 19.3 | 26 | 14.2 | 50 | 23.8 | |
Smoking | 0.427 | ||||||
No | 374 | 95.2 | 172 | 94 | 202 | 96.2 | |
Yes | 18 | 4.6 | 10 | 5.5 | 8 | 3.8 | |
Missing | 1 | 0.3 | 1 | 0.5 | 0 | 0 | |
Residential exposure to ETS | 0.809 | ||||||
No | 351 | 89.3 | 165 | 90.2 | 186 | 88.6 | |
Yes | 40 | 10.2 | 18 | 9.8 | 22 | 10.5 | |
Missing | 2 | 0.5 | 0 | 0 | 2 | 1 | |
Recent health complaints | 0.297 | ||||||
No | 277 | 70.5 | 134 | 73.2 | 143 | 68.1 | |
Yes | 115 | 29.3 | 49 | 26.8 | 66 | 31.4 | |
Missing | 1 | 0.3 | 0 | 0 | 1 | 0.5 | |
Season of sampling | 0.001 | ||||||
Winter | 123 | 31.3 | 48 | 26.2 | 75 | 35.7 | |
Spring | 180 | 45.8 | 110 | 60.1 | 70 | 33.3 | |
Summer | - | - | - | - | - | - | |
Fall | 90 | 22.9 | 25 | 13.7 | 65 | 31 | |
2-day mean temperature (°C) | 0.001 | ||||||
<6 | 145 | 36.9 | 51 | 27.9 | 94 | 44.8 | |
6−12 | 137 | 34.9 | 58 | 31.7 | 79 | 37.6 | |
>12 | 111 | 28.2 | 74 | 40.4 | 37 | 17.6 |
Biomarker | All (n = 393) | Boys (n = 183) | Girls (n = 210) | |||
---|---|---|---|---|---|---|
GM (95% CI) | p25 | p75 | GM (95% CI) | GM (95% CI) | p-Value | |
OH-PAHs (µg/L) a | ||||||
2-OHNa * | 4.04 (3.70, 4.41) | 2.15 | 7.07 | 3.48 (3.07, 3.95) | 4.60 (4.08, 5.18) | 0.002 |
2,3-OHFl * | 0.209 (0.197, 0.221) | 0.144 | 0.277 | 0.207 (0.190, 0.224) | 0.211 (0.195, 0.228) | 0.743 |
2-OHPH | 0.074 (0.069, 0.078) | 0.051 | 0.101 | 0.078 (0.072, 0.085) | 0.070 (0.065, 0.076) | 0.06 |
3-OHPH | 0.073 (0.069, 0.078) | 0.052 | 0.099 | 0.077 (0.071, 0.084) | 0.070 (0.065, 0.075) | 0.056 |
1,9-OHPH | 0.111 (0.104, 0.118) | 0.074 | 0.149 | 0.107 (0.098, 0.116) | 0.115 (0.105, 0.126) | 0.252 |
1-OHPy ** | 0.067 (0.063, 0.074) | 0.048 | 0.096 | 0.065 (0.060, 0.071) | 0.069 (0.063, 0.074) | 0.342 |
ΣOH-PAH (µmol/L) a,** | 0.032 (0.029, 0.035) | 0.018 | 0.052 | 0.028 (0.025, 0.032) | 0.036 (0.032, 0.040) | 0.004 |
Effect biomarkers | ||||||
HCC (pg/mg hair) | 3.07 (2.84, 3.31) | 2.09 | 4.38 | 2.85 (2.55, 3.19) | 3.26 (2.94, 3.62) | 0.083 |
Leucocytes (cells/µL) | 6744 (6583, 6910) | 5675 | 7925 | 6471 (6236, 6715) | 6991 (6775, 7215) | 0.002 |
Neutrophils (cells/µL) | 3535 (3403, 3672) | 2757 | 4636 | 3186 (3016, 3366) | 3870 (3682, 4068) | 0.002 |
Lymphocytes (cells/µL) | 2250 (2195, 2307) | 1941 | 2627 | 2297 (2216, 2381) | 2210 (2136, 2287) | 0.124 |
Monocytes (cells/µL) | 562 (546, 579) | 458 | 692 | 570 (547, 594) | 555 (533, 578) | 0.373 |
NLR | 1.57 (1.50, 1.64) | 1.19 | 2.1 | 1.39 (1.31, 1.47) | 1.75 (1.65, 1.86) | <0.001 |
8-oxodG (µg/L) a | 16.90 (16.19, 17.65) | 13.41 | 21.43 | 16.80 (15.85, 17.80) | 17.00 (15.95, 18.10) | 0.790 |
OH-PAHs | Model I | Model II | Model III | |||
---|---|---|---|---|---|---|
n | β (95% CI) | n | β (95% CI) | n | β (95% CI) | |
2-OHNa | 392 | 1.00 (0.94, 1.06) | 386 | 0.98 (0.92, 1.05) | 384 | 0.98 (0.92, 1.05) |
2,3-OHFl | 392 | 1.08 (0.98, 1.18) | 386 | 1.05 (0.95, 1.15) | 384 | 1.05 (0.95, 1.17) |
2-OHPH | 393 | 1.05 (0.96, 1.15) | 387 | 1.01 (0.92, 1.12) | 385 | 1.03 (0.93, 1.13) |
3-OHPH | 393 | 1.06 (0.96, 1.17) | 387 | 1.05 (0.95, 1.16) | 385 | 1.06 (0.95, 1.17) |
1,9-OHPH | 393 | 1.03 (0.95, 1.12) | 387 | 1.01 (0.93, 1.10) | 385 | 1.02 (0.94, 1.12) |
1-OHPy | 391 | 1.12 (1.02, 1.23) | 385 | 1.12 (1.02, 1.23) | 383 | 1.13 (1.03, 1.24) |
ΣOH-PAH | 391 | 1.02 (0.98, 1.06) | 385 | 1.02 (0.98, 1.06) | 383 | 1.02 (0.98, 1.06) |
OH-PAHs | Model I | Model II | Model III | |||
---|---|---|---|---|---|---|
n | β (95% CI) | n | β (95% CI) | n | β (95% CI) | |
Leukocytes | ||||||
2-OHNa | 392 | 1.00 (0.98, 1.02) | 386 | 1.00 (0.98, 1.02) | 384 | 1.00 (0.98, 1.02) |
2,3-OHFl | 392 | 1.02 (0.99, 1.05) | 386 | 1.01 (0.98, 1.05) | 384 | 1.01 (0.98, 1.04) |
2-OHPH | 393 | 1.03 (1.00 1.07) | 387 | 1.03 (1.00, 1.07) | 385 | 1.03 (1.00, 1.06) |
3-OHPH | 393 | 1.01 (0.98, 1.04) | 387 | 1.01 (0.97, 1.04) | 385 | 1.00 (0.97, 1.04) |
1,9-OHPH | 393 | 0.99 (0.96, 1.02) | 387 | 0.99 (0.96, 1.01) | 385 | 0.99 (0.96, 1.01) |
1-OHPy | 391 | 1.00 (0.98, 1.03) | 385 | 1.00 (0.97, 1.03) | 383 | 1.00 (0.97, 1.03) |
ΣOH-PAH | 391 | 1.00 (0.98, 1.06) | 385 | 1.00 (0.98, 1.02) | 383 | 1.00 (0.98, 1.02) |
Neutrophils | ||||||
2-OHNa | 392 | 1.01 (0.98, 1.04) | 386 | 1.01 (0.98, 1.04) | 384 | 1.00 (0.97, 1.04) |
2,3-OHFl | 392 | 1.04 (1.00, 1.09) | 386 | 1.04 (0.99, 1.09) | 384 | 1.03 (0.98, 1.09) |
2-OHPH | 393 | 1.06 (1.02, 1.11) | 387 | 1.06 (1.01, 1.11) | 385 | 1.06 (1.01, 1.11) |
3-OHPH | 393 | 1.03 (0.98, 1.08) | 387 | 1.02 (0.98, 1.08) | 385 | 1.02 (0.97, 1.07) |
1,9-OHPH | 393 | 1.00 (0.96, 1.04) | 387 | 0.99 (0.95, 1.04) | 385 | 0.99 (0.95, 1.04) |
1-OHPy | 391 | 1.02 (0.98, 1.07) | 385 | 1.02 (0.97, 1.07) | 383 | 1.02 (0.97, 1.06) |
ΣOH-PAH | 391 | 1.01 (0.98, 1.04) | 385 | 1.01 (0.98, 1.04) | 383 | 1.01 (0.98, 1.04) |
Lymphocytes | ||||||
2-OHNa | 392 | 0.99 (0.97, 1.01) | 386 | 0.99 (0.97, 1.01) | 384 | 0.99 (0.97, 1.01) |
2,3-OHFl | 392 | 0.98 (0.95, 1.01) | 386 | 0.98 (0.95, 1.01) | 384 | 0.97 (0.94, 1.00) |
2-OHPH | 393 | 0.99 (0.96, 1.02) | 387 | 0.98 (0.95, 1.02) | 385 | 0.98 (0.95, 1.01) |
3-OHPH | 393 | 0.98 (0.94, 1.01) | 387 | 0.97 (0.94, 1.00) | 385 | 0.97 (0.94, 1.00) |
1,9-OHPH | 393 | 0.98 (0.95, 1.01) | 387 | 0.97 (0.94, 1.00) | 385 | 0.97 (0.94, 1.00) |
1-OHPy | 391 | 0.98 (0.95, 1.21) | 385 | 0.97 (0.94, 1.00) | 383 | 0.97 (0.94, 1.01) |
ΣOH-PAH | 391 | 0.99 (0.97, 1.01) | 385 | 0.99 (0.97, 1.02) | 383 | 0.99 (0.97, 1.01) |
Monocytes | ||||||
2-OHNa | 392 | 0.98 (0.96, 1.01) | 386 | 0.98 (0.96, 1.01) | 384 | 0.98 (0.96, 1.00) |
2,3-OHFl | 392 | 1.00 (0.96, 1.03) | 386 | 1.00 (0.96, 1.04) | 384 | 1.00 (0.96, 1.04) |
2-OHPH | 393 | 1.02 (0.98, 1.06) | 387 | 1.02 (0.98, 1.06) | 385 | 1.02 (0.98, 1.06) |
3-OHPH | 393 | 1.00 (0.97, 1.04) | 387 | 1.00 (0.96, 1.04) | 385 | 1.00 (0.96, 1.04) |
1,9-OHPH | 393 | 0.98 (0.95, 1.02) | 387 | 0.98 (0.95, 1.02) | 385 | 0.98 (0.95, 1.02) |
1-OHPy | 391 | 1.00 (0.97, 1.04) | 385 | 1.00 (0.97, 1.04) | 383 | 1.00 (0.97, 1.04) |
ΣOH-PAH | 391 | 0.98 (0.96, 1.01) | 385 | 0.98 (0.96, 1.01) | 383 | 0.98 (0.96, 1.01) |
Neutrophil–lymphocyte ratio (NLR) | ||||||
2-OHNa | 392 | 1.01 (0.98, 1.05) | 386 | 1.01 (0.98, 1.05) | 384 | 1.01 (0.98, 1.05) |
2,3-OHFl | 392 | 1.06 (1.01, 1.12) | 386 | 1.06 (1.01, 1.12) | 384 | 1.06 (1.01, 1.13) |
2-OHPH | 393 | 1.08 (1.02, 1.13) | 387 | 1.08 (1.02, 1.14) | 385 | 1.08 (1.02, 1.14) |
3-OHPH | 393 | 1.05 (0.99, 1.11) | 387 | 1.05 (1.00, 1.11) | 385 | 1.05 (1.00, 1.12) |
1,9-OHPH | 393 | 1.02 (0.97, 1.06) | 387 | 1.02 (0.98, 1.07) | 385 | 1.02 (0.97, 1.07) |
1-OHPy | 391 | 1.04 (0.99, 1.10) | 385 | 1.04 (0.99, 1.09) | 383 | 1.04 (0.99, 1.10) |
ΣOH-PAH | 391 | 1.02 (0.98, 1.06) | 385 | 1.02 (0.98, 1.06) | 383 | 1.02 (0.98, 1.06) |
OH_PAHs | Model I | Model II | Model III | |||
---|---|---|---|---|---|---|
n | β (95% CI) | n | β (95% CI) | n | β (95% CI) | |
2-OHNa | 392 | 1.02 (0.99, 1.05) | 386 | 1.02 (0.99, 1.05) | 384 | 1.02 (0.98, 1.05) |
2,3-OHFl | 392 | 1.04 (0.99, 1.10) | 386 | 1.04 (1.00, 1.11) | 384 | 1.04 (0.98, 1.10) |
2-OHPH | 393 | 1.07 (1.02, 1.12) | 387 | 1.08 (1.03, 1.14) | 385 | 1.08 (1.02, 1.14) |
3-OHPH | 393 | 1.05 (1.00, 1.11) | 387 | 1.06 (1.01, 1.12) | 385 | 1.06 (1.00, 1.12) |
1,9-OHPH | 393 | 1.00 (0.96, 1.05) | 387 | 1.01 (0.97, 1.06) | 385 | 1.01 (0.96, 1.06) |
1-OHPy | 391 | 1.07 (1.02, 1.12) | 385 | 1.08 (1.03, 1.13) | 383 | 1.07 (1.02, 1.13) |
ΣOH-PAH | 391 | 1.02 (0.99, 1.06) | 385 | 1.02 (0.99, 1.06) | 383 | 1.02 (0.98, 1.06) |
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Verheyen, V.J.; Remy, S.; Govarts, E.; Colles, A.; Rodriguez Martin, L.; Koppen, G.; Voorspoels, S.; Bruckers, L.; Bijnens, E.M.; Vos, S.; et al. Urinary Polycyclic Aromatic Hydrocarbon Metabolites Are Associated with Biomarkers of Chronic Endocrine Stress, Oxidative Stress, and Inflammation in Adolescents: FLEHS-4 (2016–2020). Toxics 2021, 9, 245. https://doi.org/10.3390/toxics9100245
Verheyen VJ, Remy S, Govarts E, Colles A, Rodriguez Martin L, Koppen G, Voorspoels S, Bruckers L, Bijnens EM, Vos S, et al. Urinary Polycyclic Aromatic Hydrocarbon Metabolites Are Associated with Biomarkers of Chronic Endocrine Stress, Oxidative Stress, and Inflammation in Adolescents: FLEHS-4 (2016–2020). Toxics. 2021; 9(10):245. https://doi.org/10.3390/toxics9100245
Chicago/Turabian StyleVerheyen, Veerle J., Sylvie Remy, Eva Govarts, Ann Colles, Laura Rodriguez Martin, Gudrun Koppen, Stefan Voorspoels, Liesbeth Bruckers, Esmée M. Bijnens, Stijn Vos, and et al. 2021. "Urinary Polycyclic Aromatic Hydrocarbon Metabolites Are Associated with Biomarkers of Chronic Endocrine Stress, Oxidative Stress, and Inflammation in Adolescents: FLEHS-4 (2016–2020)" Toxics 9, no. 10: 245. https://doi.org/10.3390/toxics9100245